HHS Public Access Author manuscript Author Manuscript
Am J Prev Med. Author manuscript; available in PMC 2017 October 01. Published in final edited form as: Am J Prev Med. 2016 October ; 51(4): e107–e115. doi:10.1016/j.amepre.2016.02.025.
Racial/Ethnic Disparities in Colorectal Cancer Screening Across Healthcare Systems Andrea N. Burnett-Hartman, PhD1,2, Shivan J. Mehta, MD, MBA3, Yingye Zheng, PhD2, Nirupa R. Ghai, PhD4, Dale McLerran, MS2, Jessica Chubak, PhD5, Virginia P. Quinn, PhD4, Celette Sugg Skinner, PhD7, Douglas A. Corley, MD, PhD6, John Inadomi, MD8, and Chyke A. Doubeni, MD, MPH9 on behalf of the PROSPR Consortium
Author Manuscript
1Institute 2Fred
for Health Research, Kaiser Permanente Colorado, Denver, Colorado
Hutchinson Cancer Research Center, Seattle, Washington
3Division
of Gastroenterology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania
4Department
of Research and Evaluation, Kaiser Permanente Southern California, Pasadena,
California 5Group
Health Research Institute, Seattle, Washington
6Division
of Research, Kaiser Permanente Northern California, Oakland, California
7University
Author Manuscript
of Texas Southwestern Medical Center and the Harold C. Simmons Comprehensive Cancer Center, Dallas, Texas
8Division
of Gastroenterology, University of Washington, School of Medicine, Seattle, Washington
9Department
of Family Medicine and Community Health, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania
Abstract Introduction—Racial/ethnic disparities in colorectal cancer (CRC) screening and diagnostic testing present challenges to CRC prevention programs. Thus, it is important to understand how differences in CRC screening approaches between healthcare systems are associated with racial/ ethnic disparities.
Author Manuscript
Methods—This was a retrospective cohort study of patients aged 50–75 years who were members of the Population-based Research Optimizing Screening through Personalized Regimens cohort from 2010 to 2012. Data on race/ethnicity, CRC screening, and diagnostic testing came from medical records. Data collection occurred in 2014 and analysis in 2015. Logistic regression
Address correspondence to: Andrea N. Burnett-Hartman, PhD, 10056 E Harvard Ave., Ste. 300, Denver CO 80231. [email protected]. No financial disclosures were reported by the authors of this paper. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Burnett-Hartman et al.
Page 2
Author Manuscript
models were used to calculate AORs and 95% CIs comparing completion of CRC screening between racial/ethnic groups. Analyses were stratified by healthcare system to assess differences between systems. Results—There were 1,746,714 participants across four healthcare systems. Compared with nonHispanic whites (whites), odds of completing CRC screening were lower for non-Hispanic blacks (blacks) in healthcare systems with high screening rates (AOR=0.86, 95% CI=0.84, 0.88) but similar between blacks and whites in systems with lower screening rates (AOR=1.01, 95% CI=0.93, 1.09). Compared with whites, American Indian/Alaskan Natives had lower odds of completing CRC screening across all healthcare systems (AOR=0.76, 95% CI=0.72, 0.81). Hispanics had similar odds of CRC screening (AOR=0.99, 95% CI=0.98, 1.00) and Asian/Pacific Islanders had higher odds of CRC screening (AOR=1.16, 95% CI=1.15, 1.18) versus whites.
Author Manuscript
Conclusions—Racial/ethnic differences in CRC screening vary across healthcare systems, particularly for blacks, and may be more pronounced in systems with intensive CRC screening approaches.
Introduction Despite effective strategies for prevention, early detection, and treatment,1–9 there continue to be differences in colorectal cancer (CRC) incidence and survival by race/ethnicity.10–14 Specifically, African Americans have higher CRC incidence and lower 5-year survival rates than other racial/ethnic groups.10,11 This disparity may, in part, be due to differences in the utilization of CRC screening or access to health care.12,15,16
Author Manuscript
Utilization of CRC screening and access to health care can be influenced by many factors. Based on the Health Beliefs Model, CRC screening behaviors vary by race/ethnicity because different racial/ethnic groups have distinct beliefs about the risks and benefits of CRC screening.17 These beliefs may interact with system-level factors, such as the healthcare delivery system’s approach to CRC screening. Different approaches to CRC screening include: relying on providers to recommend screening during office visits, mailing reminder letters, and sending stool-based test kits to patients who are due for screening.18–20 Although some studies have evaluated health disparities in national or regional screening programs,21–23 few have examined racial/ethnic differences in the receipt of CRC screening and diagnostic testing between health systems in the U.S. that use different screening approaches.24,25
Author Manuscript
Additionally, stool-based testing, including the fecal immunochemical test (FIT) and guaiacbased fecal occult blood test (gFOBT), is an important part of many CRC screening programs, and requires timely follow-up of positive stool-based test results with a colonoscopy to complete the screening episode. Prior studies that only measure initiation of CRC screening, but do not include follow-up of abnormal results, may overestimate CRC screening in the population and miss potential differences in CRC screening completion and diagnostic testing between groups. The underlying hypothesis is that the association between race/ethnicity and colorectal cancer screening completion differs between healthcare systems that use different
Am J Prev Med. Author manuscript; available in PMC 2017 October 01.
Burnett-Hartman et al.
Page 3
Author Manuscript
approaches to CRC screening outreach. Thus, this study evaluates racial/ethnic differences in receipt of CRC screening and follow-up diagnostic testing across four diverse health systems and patient populations.
Methods Study Setting and Population
Author Manuscript
This study was conducted as part of the National Cancer Institute–funded consortium Population-based Research Optimizing Screening through Personalized Regimens (PROSPR). The overall aim of PROSPR is to conduct multisite, coordinated, transdisciplinary research to evaluate and improve cancer screening processes. The ten PROSPR Research Centers reflect the diversity of U.S. delivery system organizations. The PROSPR CRC sites for this study were Group Health Research Institute (GH), the Kaiser Permanente consortium (Kaiser Permanente Northern California [KPNC] and Kaiser Permanente Southern California [KPSC]), and the Parkland Health & Hospital System/ University of Texas Southwestern Medical Center (PHHS-UTSW).26
Author Manuscript
During the study period, the healthcare delivery systems employed different approaches to CRC screening; all centers offered endoscopic and stool-based tests.26 However, how these tests were offered varied by system. GH patients received take-home gFOBT/FIT test kits or recommendations for endoscopic screening during office visits. Patients also received annual reminder letters about screening and follow-up calls and could request that a stool-based test kit be mailed to them. KPNC and KPSC had intensive programs that relied on mailed FIT tests for all members not up to date with screening, regardless of whether or not members requested a test or had an office visit.18 PHHS-UTSW, the safety net provider for Dallas County residents, relied on providers to recommend and order tests based on patient preference. The study population included screening-eligible cohort members from January 1, 2010 to December 31, 2012. For GH, KPNC, and KPSC, eligible patients included those who were aged 50–75 years. PHHS-UTSW patients included in the study had at least one visit with a Parkland primary care provider in 2010–2012, and were aged 50–64 years. This upper age limit of 64 years for PHHS-UTSW was due to incomplete data capture on Medicare-eligible patients.
Author Manuscript
Patients with a known history of colectomy; CRC prior to cohort entry; or incomplete data on race/ethnicity, cohort entry date, or sex were excluded. The authors also excluded those with a history of colonoscopy within 10 years or sigmoidoscopy within 5 years prior to cohort entry, because these cohort members were considered up to date with CRC screening.27 Protocols and study procedures for PROSPR were approved by the IRBs at each research center and at the Fred Hutchinson Cancer Research Center, which manages the pooled PROSPR data. Data Collection Each healthcare system in the PROSPR CRC consortium uses comprehensive electronic medical record systems and administrative databases that were used to collect demographic
Am J Prev Med. Author manuscript; available in PMC 2017 October 01.
Burnett-Hartman et al.
Page 4
Author Manuscript
information (e.g., age, sex, and race and ethnicity) and track patient utilization, health insurance, orders, test results, and pathology results.26 Cohort members were followed up for procedures and tests occurring from the time of cohort entry until the first of the following events: 18 months of follow-up; December 31, 2012; death; disenrollment; or in the case of PHHS-UTSW, known relocation outside of Dallas County. Prior history of sigmoidoscopy and colonoscopy, including time since the last procedure, were retrospectively collected from electronic databases, going back to 2006 for GH, 1999 for KPNC and KPSC, and 2010 for PHHS-UTSW. The study also collected data on continuous months of enrollment in the healthcare system (allowing for a 90-day gap in enrollment) prior to cohort entry and demographic information. Data collection occurred in 2014.
Author Manuscript
Measures The key variable of interest, race/ethnicity, was generally obtained from patient self-report during health system enrollment or at office visits. Race/ethnicity was categorized as nonHispanic white (white), non-Hispanic black (black), Hispanic, Asian/Pacific Islander (API), American Indian/Alaska Native (AI/AN), or multiple/other.26 The primary outcome of interest was completion of an incident CRC screening episode. This was defined as having at least one of the following during the first 18 months after entry into the PROSPR cohort:
Author Manuscript
1.
screening colonoscopy;
2.
sigmoidoscopy;
3.
gFOBT or FIT with a negative result; or
4.
gFOBT or FIT with a positive result followed by a colonoscopy within 90 days.
Current Procedural Terminology, Healthcare Common Procedure Coding System, and lab codes were used to ascertain receipt of colonoscopy, sigmoidoscopy, and FIT or gFOBT. FIT and gFOBT results were derived from laboratory databases. Statistical Analysis Analyses were conducted in 2015 using the pooled data and also separately for each healthcare system. SAS, version 9.3 was used for all analyses.
Author Manuscript
Logistic regression models were used to calculate AORs and 95% CIs comparing completion of an incident CRC screening episode within 18 months of follow-up between each race/ethnic group and whites. All patients who completed incident screening within the first 18 months of follow-up were included in the models irrespective of follow-up duration, but those without incident screening and
Am J Prev Med. Author manuscript; available in PMC 2017 October 01. Published in final edited form as: Am J Prev Med. 2016 October ; 51(4): e107–e115. doi:10.1016/j.amepre.2016.02.025.
Racial/Ethnic Disparities in Colorectal Cancer Screening Across Healthcare Systems Andrea N. Burnett-Hartman, PhD1,2, Shivan J. Mehta, MD, MBA3, Yingye Zheng, PhD2, Nirupa R. Ghai, PhD4, Dale McLerran, MS2, Jessica Chubak, PhD5, Virginia P. Quinn, PhD4, Celette Sugg Skinner, PhD7, Douglas A. Corley, MD, PhD6, John Inadomi, MD8, and Chyke A. Doubeni, MD, MPH9 on behalf of the PROSPR Consortium
Author Manuscript
1Institute 2Fred
for Health Research, Kaiser Permanente Colorado, Denver, Colorado
Hutchinson Cancer Research Center, Seattle, Washington
3Division
of Gastroenterology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania
4Department
of Research and Evaluation, Kaiser Permanente Southern California, Pasadena,
California 5Group
Health Research Institute, Seattle, Washington
6Division
of Research, Kaiser Permanente Northern California, Oakland, California
7University
Author Manuscript
of Texas Southwestern Medical Center and the Harold C. Simmons Comprehensive Cancer Center, Dallas, Texas
8Division
of Gastroenterology, University of Washington, School of Medicine, Seattle, Washington
9Department
of Family Medicine and Community Health, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania
Abstract Introduction—Racial/ethnic disparities in colorectal cancer (CRC) screening and diagnostic testing present challenges to CRC prevention programs. Thus, it is important to understand how differences in CRC screening approaches between healthcare systems are associated with racial/ ethnic disparities.
Author Manuscript
Methods—This was a retrospective cohort study of patients aged 50–75 years who were members of the Population-based Research Optimizing Screening through Personalized Regimens cohort from 2010 to 2012. Data on race/ethnicity, CRC screening, and diagnostic testing came from medical records. Data collection occurred in 2014 and analysis in 2015. Logistic regression
Address correspondence to: Andrea N. Burnett-Hartman, PhD, 10056 E Harvard Ave., Ste. 300, Denver CO 80231. [email protected]. No financial disclosures were reported by the authors of this paper. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Burnett-Hartman et al.
Page 2
Author Manuscript
models were used to calculate AORs and 95% CIs comparing completion of CRC screening between racial/ethnic groups. Analyses were stratified by healthcare system to assess differences between systems. Results—There were 1,746,714 participants across four healthcare systems. Compared with nonHispanic whites (whites), odds of completing CRC screening were lower for non-Hispanic blacks (blacks) in healthcare systems with high screening rates (AOR=0.86, 95% CI=0.84, 0.88) but similar between blacks and whites in systems with lower screening rates (AOR=1.01, 95% CI=0.93, 1.09). Compared with whites, American Indian/Alaskan Natives had lower odds of completing CRC screening across all healthcare systems (AOR=0.76, 95% CI=0.72, 0.81). Hispanics had similar odds of CRC screening (AOR=0.99, 95% CI=0.98, 1.00) and Asian/Pacific Islanders had higher odds of CRC screening (AOR=1.16, 95% CI=1.15, 1.18) versus whites.
Author Manuscript
Conclusions—Racial/ethnic differences in CRC screening vary across healthcare systems, particularly for blacks, and may be more pronounced in systems with intensive CRC screening approaches.
Introduction Despite effective strategies for prevention, early detection, and treatment,1–9 there continue to be differences in colorectal cancer (CRC) incidence and survival by race/ethnicity.10–14 Specifically, African Americans have higher CRC incidence and lower 5-year survival rates than other racial/ethnic groups.10,11 This disparity may, in part, be due to differences in the utilization of CRC screening or access to health care.12,15,16
Author Manuscript
Utilization of CRC screening and access to health care can be influenced by many factors. Based on the Health Beliefs Model, CRC screening behaviors vary by race/ethnicity because different racial/ethnic groups have distinct beliefs about the risks and benefits of CRC screening.17 These beliefs may interact with system-level factors, such as the healthcare delivery system’s approach to CRC screening. Different approaches to CRC screening include: relying on providers to recommend screening during office visits, mailing reminder letters, and sending stool-based test kits to patients who are due for screening.18–20 Although some studies have evaluated health disparities in national or regional screening programs,21–23 few have examined racial/ethnic differences in the receipt of CRC screening and diagnostic testing between health systems in the U.S. that use different screening approaches.24,25
Author Manuscript
Additionally, stool-based testing, including the fecal immunochemical test (FIT) and guaiacbased fecal occult blood test (gFOBT), is an important part of many CRC screening programs, and requires timely follow-up of positive stool-based test results with a colonoscopy to complete the screening episode. Prior studies that only measure initiation of CRC screening, but do not include follow-up of abnormal results, may overestimate CRC screening in the population and miss potential differences in CRC screening completion and diagnostic testing between groups. The underlying hypothesis is that the association between race/ethnicity and colorectal cancer screening completion differs between healthcare systems that use different
Am J Prev Med. Author manuscript; available in PMC 2017 October 01.
Burnett-Hartman et al.
Page 3
Author Manuscript
approaches to CRC screening outreach. Thus, this study evaluates racial/ethnic differences in receipt of CRC screening and follow-up diagnostic testing across four diverse health systems and patient populations.
Methods Study Setting and Population
Author Manuscript
This study was conducted as part of the National Cancer Institute–funded consortium Population-based Research Optimizing Screening through Personalized Regimens (PROSPR). The overall aim of PROSPR is to conduct multisite, coordinated, transdisciplinary research to evaluate and improve cancer screening processes. The ten PROSPR Research Centers reflect the diversity of U.S. delivery system organizations. The PROSPR CRC sites for this study were Group Health Research Institute (GH), the Kaiser Permanente consortium (Kaiser Permanente Northern California [KPNC] and Kaiser Permanente Southern California [KPSC]), and the Parkland Health & Hospital System/ University of Texas Southwestern Medical Center (PHHS-UTSW).26
Author Manuscript
During the study period, the healthcare delivery systems employed different approaches to CRC screening; all centers offered endoscopic and stool-based tests.26 However, how these tests were offered varied by system. GH patients received take-home gFOBT/FIT test kits or recommendations for endoscopic screening during office visits. Patients also received annual reminder letters about screening and follow-up calls and could request that a stool-based test kit be mailed to them. KPNC and KPSC had intensive programs that relied on mailed FIT tests for all members not up to date with screening, regardless of whether or not members requested a test or had an office visit.18 PHHS-UTSW, the safety net provider for Dallas County residents, relied on providers to recommend and order tests based on patient preference. The study population included screening-eligible cohort members from January 1, 2010 to December 31, 2012. For GH, KPNC, and KPSC, eligible patients included those who were aged 50–75 years. PHHS-UTSW patients included in the study had at least one visit with a Parkland primary care provider in 2010–2012, and were aged 50–64 years. This upper age limit of 64 years for PHHS-UTSW was due to incomplete data capture on Medicare-eligible patients.
Author Manuscript
Patients with a known history of colectomy; CRC prior to cohort entry; or incomplete data on race/ethnicity, cohort entry date, or sex were excluded. The authors also excluded those with a history of colonoscopy within 10 years or sigmoidoscopy within 5 years prior to cohort entry, because these cohort members were considered up to date with CRC screening.27 Protocols and study procedures for PROSPR were approved by the IRBs at each research center and at the Fred Hutchinson Cancer Research Center, which manages the pooled PROSPR data. Data Collection Each healthcare system in the PROSPR CRC consortium uses comprehensive electronic medical record systems and administrative databases that were used to collect demographic
Am J Prev Med. Author manuscript; available in PMC 2017 October 01.
Burnett-Hartman et al.
Page 4
Author Manuscript
information (e.g., age, sex, and race and ethnicity) and track patient utilization, health insurance, orders, test results, and pathology results.26 Cohort members were followed up for procedures and tests occurring from the time of cohort entry until the first of the following events: 18 months of follow-up; December 31, 2012; death; disenrollment; or in the case of PHHS-UTSW, known relocation outside of Dallas County. Prior history of sigmoidoscopy and colonoscopy, including time since the last procedure, were retrospectively collected from electronic databases, going back to 2006 for GH, 1999 for KPNC and KPSC, and 2010 for PHHS-UTSW. The study also collected data on continuous months of enrollment in the healthcare system (allowing for a 90-day gap in enrollment) prior to cohort entry and demographic information. Data collection occurred in 2014.
Author Manuscript
Measures The key variable of interest, race/ethnicity, was generally obtained from patient self-report during health system enrollment or at office visits. Race/ethnicity was categorized as nonHispanic white (white), non-Hispanic black (black), Hispanic, Asian/Pacific Islander (API), American Indian/Alaska Native (AI/AN), or multiple/other.26 The primary outcome of interest was completion of an incident CRC screening episode. This was defined as having at least one of the following during the first 18 months after entry into the PROSPR cohort:
Author Manuscript
1.
screening colonoscopy;
2.
sigmoidoscopy;
3.
gFOBT or FIT with a negative result; or
4.
gFOBT or FIT with a positive result followed by a colonoscopy within 90 days.
Current Procedural Terminology, Healthcare Common Procedure Coding System, and lab codes were used to ascertain receipt of colonoscopy, sigmoidoscopy, and FIT or gFOBT. FIT and gFOBT results were derived from laboratory databases. Statistical Analysis Analyses were conducted in 2015 using the pooled data and also separately for each healthcare system. SAS, version 9.3 was used for all analyses.
Author Manuscript
Logistic regression models were used to calculate AORs and 95% CIs comparing completion of an incident CRC screening episode within 18 months of follow-up between each race/ethnic group and whites. All patients who completed incident screening within the first 18 months of follow-up were included in the models irrespective of follow-up duration, but those without incident screening and
